Dipeptidyl peptidase-4 inhibition by gemigliptin prevents abnormal vascular remodeling via NF-E2-related factor 2 activation

Vascular Pharmacology

Volumn 73, Issue , 2015, Pages 11-19

  Choi, Seung Hee ^a   Park, Sungmi ^a   Oh, Chang Joo ^a   Leem, Jaechan ^a   Park, Keun Gyu ^a,b   Lee, In Kyu ^a,b  

^a Kyungpook National University   (South Korea)

^b Kyungpook National University School of Medicine   (South Korea)

Author keywords

Anti oxidative stress; Cardiovascular diseases; Carotid artery; Cell cycle; P62 Keap1 Nrf2 pathway; Reactive oxygen species

Indexed keywords

DIPEPTIDYL PEPTIDASE IV; GELATINASE A; GEMIGLIPTIN; KELCH LIKE ECH ASSOCIATED PROTEIN 1; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; PROTEIN P62; RETINOBLASTOMA PROTEIN; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR NRF2; TUMOR NECROSIS FACTOR ALPHA; VASCULAR CELL ADHESION MOLECULE 1; CELL ADHESION MOLECULE; DIPEPTIDYL PEPTIDASE IV INHIBITOR; DPP4 PROTEIN, MOUSE; DPP4 PROTEIN, RAT; LC15-0444; MMP2 PROTEIN, RAT; NFE2L2 PROTEIN, MOUSE; NFE2L2 PROTEIN, RAT; PIPERIDONE DERIVATIVE; PYRIMIDINE DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIPROLIFERATIVE ACTIVITY; ARTICLE; CAROTID ARTERY LIGATION; CELL MIGRATION; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; G1 PHASE CELL CYCLE CHECKPOINT; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; RAT; VASCULAR REMODELING; VASCULAR SMOOTH MUSCLE CELL; ANIMAL; C57BL MOUSE; CAROTID ARTERY INJURIES; CELL MOTION; DISEASE MODEL; DOSE RESPONSE; DRUG EFFECTS; ENZYMOLOGY; GENETIC TRANSFECTION; GENETICS; HEK293 CELL LINE; HUMAN; HYPERPLASIA; METABOLISM; NEOINTIMA; PATHOLOGY; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SMOOTH MUSCLE CELL; SPRAGUE DAWLEY RAT; TIME FACTOR; VASCULAR SMOOTH MUSCLE;

ANIMALS; CAROTID ARTERY INJURIES; CELL ADHESION MOLECULES; CELL MOVEMENT; CELL PROLIFERATION; DIPEPTIDYL PEPTIDASE 4; DIPEPTIDYL-PEPTIDASE IV INHIBITORS; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; G1 PHASE CELL CYCLE CHECKPOINTS; HEK293 CELLS; HUMANS; HYPERPLASIA; MALE; MATRIX METALLOPROTEINASE 2; MICE, INBRED C57BL; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; NEOINTIMA; NF-E2-RELATED FACTOR 2; PIPERIDONES; PYRIMIDINES; RATS, SPRAGUE-DAWLEY; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TIME FACTORS; TRANSFECTION; VASCULAR REMODELING;

EID: 84941737200     PISSN: 15371891     EISSN: 18793649     Source Type: Journal    
DOI: 10.1016/j.vph.2015.07.005     Document Type: Article

References (43)

1. Fadini G.P., Avogaro A. Cardiovascular effects of DPP-4 inhibition: beyond GLP-1. Vasc. Pharmacol. 2011, 55:10-16.
2. Kjems L.L., Holst J.J., Volund A., Madsbad S. The influence of GLP-1 on glucose-stimulated insulin secretion: effects on beta-cell sensitivity in type 2 and nondiabetic subjects. Diabetes 2003, 52:380-386.
3. Flint A., Raben A., Ersboll A.K., Holst J.J., Astrup A. The effect of physiological levels of glucagon-like peptide-1 on appetite, gastric emptying, energy and substrate metabolism in obesity. Int. J. Obes. Relat. Metab. Disord. 2001, 25:781-792.
4. Parker J.A., McCullough K.A., Field B.C., Minnion J.S., Martin N.M., Ghatei M.A., Bloom S.R. Glucagon and GLP-1 inhibit food intake and increase c-fos expression in similar appetite regulating centres in the brainstem and amygdala. Int. J. Obes. (Lond.) 2013, 37:1391-1398.
5. Murthy S.N., Hilaire R.C., Casey D.B., Badejo A.M., McGee J., McNamara D.B., Kadowitz P.J., Fonseca V.A. The synthetic GLP-I receptor agonist, exenatide, reduces intimal hyperplasia in insulin resistant rats. Diab. Vasc. Dis. Res. 2010, 7:138-144.
6. Ban K., Kim K.H., Cho C.K., Sauve M., Diamandis E.P., Backx P.H., Drucker D.J., Husain M. Glucagon-like peptide (GLP)-1(9-36)amide-mediated cytoprotection is blocked by exendin(9-39) yet does not require the known GLP-1 receptor. Endocrinology 2010, 151:1520-1531.
7. Liu Q., Anderson C., Broyde A., Polizzi C., Fernandez R., Baron A., Parkes D.G. Glucagon-like peptide-1 and the exenatide analogue ac3174 improve cardiac function, cardiac remodeling, and survival in rats with chronic heart failure. Cardiovasc. Diabetol. 2010, 9:76.
8. Best J.H., Hoogwerf B.J., Herman W.H., Pelletier E.M., Smith D.B., Wenten M., Hussein M.A. Risk of cardiovascular disease events in patients with type 2 diabetes prescribed the glucagon-like peptide 1 (GLP-1) receptor agonist exenatide twice daily or other glucose-lowering therapies: a retrospective analysis of the lifelink database. Diabetes Care 2011, 34:90-95.
9. Matsubara J., Sugiyama S., Sugamura K., Nakamura T., Fujiwara Y., Akiyama E., Kurokawa H., Nozaki T., Ohba K., Konishi M., Maeda H., Izumiya Y., Kaikita K., Sumida H., Jinnouchi H., Matsui K., Kim-Mitsuyama S., Takeya M., Ogawa H. A dipeptidyl peptidase-4 inhibitor, des-fluoro-sitagliptin, improves endothelial function and reduces atherosclerotic lesion formation in apolipoprotein E-deficient mice. J. Am. Coll. Cardiol. 2012, 59:265-276.
10. Ervinna N., Mita T., Yasunari E., Azuma K., Tanaka R., Fujimura S., Sukmawati D., Nomiyama T., Kanazawa A., Kawamori R., Fujitani Y., Watada H. Anagliptin, a DPP-4 inhibitor, suppresses proliferation of vascular smooth muscles and monocyte inflammatory reaction and attenuates atherosclerosis in male apo E-deficient mice. Endocrinology 2013, 154:1260-1270.
11. Mita T., Katakami N., Shiraiwa T., Yoshii H., Onuma T., Kuribayashi N., Osonoi T., Kaneto H., Kosugi K., Umayahara Y., Yamamoto T., Matsumoto K., Yokoyama H., Tsugawa M., Gosho M., Shimomura I., Watada H. Rationale, design, and baseline characteristics of a clinical trial for prevention of atherosclerosis in patients with insulin-treated type 2 diabetes mellitus using DPP-4 inhibitor: the sitagliptin preventive study of intima-media thickness evaluation (spike). Diabetol. Metab. Syndr. 2014, 6:35.
12. Baggio L.L., Drucker D.J. Biology of incretins: GLP-1 and GIP. Gastroenterology 2007, 132:2131-2157.
13. Miyazaki M., Kato M., Tanaka K., Tanaka M., Kohjima M., Nakamura K., Enjoji M., Nakamuta M., Kotoh K., Takayanagi R. Increased hepatic expression of dipeptidyl peptidase-4 in non-alcoholic fatty liver disease and its association with insulin resistance and glucose metabolism. Mol. Med. Rep. 2012, 5:729-733.
14. Lamers D., Famulla S., Wronkowitz N., Hartwig S., Lehr S., Ouwens D.M., Eckardt K., Kaufman J.M., Ryden M., Muller S., Hanisch F.G., Ruige J., Arner P., Sell H., Eckel J. Dipeptidyl peptidase 4 is a novel adipokine potentially linking obesity to the metabolic syndrome. Diabetes 2011, 60:1917-1925.
15. Javidroozi M., Zucker S., Chen W.T. Plasma seprase and DPP4 levels as markers of disease and prognosis in cancer. Dis. Markers 2012, 32:309-320.
16. Gu N., Tsuda M., Matsunaga T., Adachi T., Yasuda K., Ishihara A., Tsuda K. Glucose regulation of dipeptidyl peptidase iv gene expression is mediated by hepatocyte nuclear factor-1alpha in epithelial intestinal cells. Clin. Exp. Pharmacol. Physiol. 2008, 35:1433-1439.
17. Bauvois B., Djavaheri-Mergny M., Rouillard D., Dumont J., Wietzerbin J. Regulation of CD26/DPPIV gene expression by interferons and retinoic acid in tumor b cells. Oncogene 2000, 19:265-272.
18. Clempus R.E., Griendling K.K. Reactive oxygen species signaling in vascular smooth muscle cells. Cardiovasc. Res. 2006, 71:216-225.
19. Brown D.I., Griendling K.K. Regulation of signal transduction by reactive oxygen species in the cardiovascular system. Circ. Res. 2015, 116:531-549.
20. Kim H.J., Kim J.Y., Lee S.J., Oh C.J., Choi Y.K., Lee H.J., Do J.Y., Kim S.Y., Kwon T.K., Choi H.S., Lee M.O., Park I.S., Park K.G., Lee K.U., Lee I.K. Alpha-lipoic acid prevents neointimal hyperplasia via induction of p38 mitogen-activated protein kinase/Nur77-mediated apoptosis of vascular smooth muscle cells and accelerates postinjury reendothelialization. Arterioscler. Thromb. Vasc. Biol. 2010, 30:2164-2172.
21. Roos T.U., Heiss E.H., Schwaiberger A.V., Schachner D., Sroka I.M., Oberan T., Vollmar A.M., Dirsch V.M. Caffeic acid phenethyl ester inhibits PDGF-induced proliferation of vascular smooth muscle cells via activation of p38 MAPK, HIF-1alpha, and heme oxygenase-1. J. Nat. Prod. 2011, 74:352-356.
22. Sung J.Y., Choi H.C. Nifedipine inhibits vascular smooth muscle cell proliferation and reactive oxygen species production through amp-activated protein kinase signaling pathway. Vasc. Pharmacol. 2012, 56:1-8.
23. Kim Y., Han J.H., Yun E., Jung S.H., Lee J.J., Song G.Y., Myung C.S. Inhibitory effect of a novel naphthoquinone derivative on proliferation of vascular smooth muscle cells through suppression of platelet-derived growth factor receptor beta tyrosine kinase. Eur. J. Pharmacol. 2014, 733:81-89.
24. Huang C.Y., Shih C.M., Tsao N.W., Lin Y.W., Huang P.H., Wu S.C., Lee A.W., Kao Y.T., Chang N.C., Nakagami H., Morishita R., Ou K.L., Hou W.C., Lin C.Y., Shyu K.G., Lin F.Y. Dipeptidyl peptidase-4 inhibitor improves neovascularization by increasing circulating endothelial progenitor cells. Br. J. Pharmacol. 2012, 167:1506-1519.
25. Zeng Y., Li C., Guan M., Zheng Z., Li J., Xu W., Wang L., He F., Xue Y. The DPP-4 inhibitor sitagliptin attenuates the progress of atherosclerosis in apolipoprotein-e-knockout mice via AMPK- and MAPK-dependent mechanisms. Cardiovasc. Diabetol. 2014, 13:32.
26. Ichikawa T., Li J., Meyer C.J., Janicki J.S., Hannink M., Cui T. Dihydro-CDDO-trifluoroethyl amide (DH404), a novel NRF2 activator, suppresses oxidative stress in cardiomyocytes. PLoS One 2009, 4:e8391.
27. Kaspar J.W., Niture S.K., Jaiswal A.K. Nrf2:Inrf2 (Keap1) signaling in oxidative stress. Free Radic. Biol. Med. 2009, 47:1304-1309.
28. Komatsu M., Kurokawa H., Waguri S., Taguchi K., Kobayashi A., Ichimura Y., Sou Y.S., Ueno I., Sakamoto A., Tong K.I., Kim M., Nishito Y., Iemura S., Natsume T., Ueno T., Kominami E., Motohashi H., Tanaka K., Yamamoto M. The selective autophagy substrate p62 activates the stress responsive transcription factor Nrf2 through inactivation of Keap1. Nat. Cell Biol. 2010, 12:213-223.
29. Kwon J., Han E., Bui C.B., Shin W., Lee J., Lee S., Choi Y.B., Lee A.H., Lee K.H., Park C., Obin M.S., Park S.K., Seo Y.J., Oh G.T., Lee H.W., Shin J. Assurance of mitochondrial integrity and mammalian longevity by the p62-Keap1-Nrf2-NQO1 cascade. EMBO Rep. 2012, 13:150-156.
30. Mukai E., Fujimoto S., Sato H., Oneyama C., Kominato R., Sato Y., Sasaki M., Nishi Y., Okada M., Inagaki N. Exendin-4 suppresses SRC activation and reactive oxygen species production in diabetic Goto-Kakizaki rat islets in an Epac-dependent manner. Diabetes 2011, 60:218-226.
31. Kumar A., Lindner V. Remodeling with neointima formation in the mouse carotid artery after cessation of blood flow. Arterioscler. Thromb. Vasc. Biol. 1997, 17:2238-2244.
32. Zhang L.N., Parkinson J.F., Haskell C., Wang Y.X. Mechanisms of intimal hyperplasia learned from a murine carotid artery ligation model. Curr. Vasc. Pharmacol. 2008, 6:37-43.
33. Kim H.J., Yoo E.K., Kim J.Y., Choi Y.K., Lee H.J., Kim J.K., Jeoung N.H., Lee K.U., Park I.S., Min B.H., Park K.G., Lee C.H., Aronow B.J., Sata M., Lee I.K. Protective role of clusterin/apolipoprotein j against neointimal hyperplasia via antiproliferative effect on vascular smooth muscle cells and cytoprotective effect on endothelial cells. Arterioscler. Thromb. Vasc. Biol. 2009, 29:1558-1564.
34. Subtil-Rodriguez A., Vazquez-Chavez E., Ceballos-Chavez M., Rodriguez-Paredes M., Martin-Subero J.I., Esteller M., Reyes J.C. The chromatin remodeller CHD8 is required for E2F-dependent transcription activation of S-phase genes. Nucleic Acids Res. 2014, 42:2185-2196.
35. Satoh K., Satoh T., Kikuchi N., Omura J., Kurosawa R., Suzuki K., Sugimura K., Aoki T., Nochioka K., Tatebe S., Miyamichi-Yamamoto S., Miura M., Shimizu T., Ikeda S., Yaoita N., Fukumoto Y., Minami T., Miyata S., Nakamura K., Ito H., Kadomatsu K., Shimokawa H. Basigin mediates pulmonary hypertension by promoting inflammation and vascular smooth muscle cell proliferation. Circ. Res. 2014, 115:738-750.
36. Chung C.H., Lin K.T., Chang C.H., Peng H.C., Huang T.F. The integrin alpha2beta1 agonist, aggretin, promotes proliferation and migration of VSMC through Nf-Kb translocation and PDGF production. Br. J. Pharmacol. 2009, 156:846-856.
37. Ha C.M., Park S., Choi Y.K., Jeong J.Y., Oh C.J., Bae K.H., Lee S.J., Kim J.H., Park K.G., Jun do Y., Lee I.K. Activation of Nrf2 by dimethyl fumarate improves vascular calcification. Vasc. Pharmacol. 2014, 63:29-36.
38. Lim S., Choi S.H., Shin H., Cho B.J., Park H.S., Ahn B.Y., Kang S.M., Yoon J.W., Jang H.C., Kim Y.B., Park K.S. Effect of a dipeptidyl peptidase-IV inhibitor, des-fluoro-sitagliptin, on neointimal formation after balloon injury in rats. PLoS One 2012, 7:e35007.
39. Goto H., Nomiyama T., Mita T., Yasunari E., Azuma K., Komiya K., Arakawa M., Jin W.L., Kanazawa A., Kawamori R., Fujitani Y., Hirose T., Watada H. Exendin-4, a glucagon-like peptide-1 receptor agonist, reduces intimal thickening after vascular injury. Biochem. Biophys. Res. Commun. 2011, 405:79-84.
40. Dai Y., Dai D., Wang X., Ding Z., Mehta J.L. DPP-4 inhibitors repress NLRP3 inflammasome and interleukin-1beta via GLP-1 receptor in macrophages through protein kinase c pathway. Cardiovasc. Drugs Ther. 2014, 28:425-432.
41. Dai Y., Wang X., Ding Z., Dai D., Mehta J.L. DPP-4 inhibitors repress foam cell formation by inhibiting scavenger receptors through protein kinase c pathway. Acta Diabetol. 2014, 51:471-478.
42. Lau A., Wang X.J., Zhao F., Villeneuve N.F., Wu T., Jiang T., Sun Z., White E., Zhang D.D. A noncanonical mechanism of Nrf2 activation by autophagy deficiency: direct interaction between Keap1 and p62. Mol. Cell. Biol. 2010, 30:3275-3285.
43. Jain A., Lamark T., Sjottem E., Larsen K.B., Awuh J.A., Overvatn A., McMahon M., Hayes J.D., Johansen T. P62/SQSTM1 is a target gene for transcription factor Nrf2 and creates a positive feedback loop by inducing antioxidant response element-driven gene transcription. J. Biol. Chem. 2010, 285:22576-22591.